2. Microbiome and Stresses
Plant metabolism is highly affected by biotic, as well as abiotic, stresses. These stresses also have a significant effect on the composition of root exudates. Field-grown plants are highly exposed to environmental stresses. Biotic stress factors are extremely harmful to plant growth and development. These factors include pathogenic fungi, bacteria, viruses, nematodes, and insects, while abiotic stress factors include temperature, drought, waterlogging, salinity, toxic organic compounds, and metal salts. These abiotic stresses also have negative effects on plant growth. There is a high chance that plants may encounter various environmental stresses at the same time. Contrarily, much rhizospheric microbiota protect plants from massive environmental stresses. The selection of plant-growth-promoting bacteria (PGPBs) depends on the range of environmental stresses. It has been observed that PGPBs play a significant role in the growth and development of plants. Under biotic and abiotic stresses, the synthesis of phytohormones such as ethylene can vary under moderate environmental stresses. In response to ethylene production, plant defensive genes are expressed to protect plants from environmental stresses. A high concentration of ethylene in plants may lead to plant senescence, chlorosis, and abscission
[21][93]. Biotic stresses often alter the composition of microbial communities associated with the stress plants. It has been reported that, in the diseased cotton plant of
Verticillium, the number of beneficial bacteria and arbuscular mycorrhizal fungi decreased, while plant pathogenic fungi increased. The relationship between the soil microbiome and the strawberry plant’s resistance against
Verticillium dahlia and
Macrophomina phaseolina has been observed. In another experiment, an alteration in the root exudate was observed due to the aphid infestation in the pepper plant. This phenomenon leads to the decreased resistance of pepper plants to aphids due to plant-recruiting rhizobacteria
[22][94]. In another study, it has been observed that compost has a significant effect on tomato plant growth and can also aid in fighting the diseases caused by
Fusarium oxysporium and
Verticillium dahlia. The added compost also helped to decrease the disease intensity caused by these pathogens. Thus, it was concluded that fungal pathogens may alter the composition of plant microbiomes, and added compost may overcome the negative effects
[23][95].
Many abiotic factors, such as drought and salinity, inhibit the crop yield and have negative effects on the crop microbiome. In yet another study, a significant difference was observed between dry-wheat land and irrigated crops. Later, it was noted that the density of the rhizosphere microbiome increases in irrigated crops
[24][96]. Thus, it can be concluded that, for the maintenance of a healthy rhizosphere microbiome, an adequate amount of water is necessary. An improvement in a drought-ridden cotton plant through a beneficial microbiome has also been observed. It was observed that the development of the sorghum root microbiome has been delayed due to drought stress. The drought stress leads to the abundance of bacteria within the microbiome. Climate change, including extreme temperatures, may affect the phyllosphere and rhizosphere microbiome of many plants. The soil microbiome is also affected by the low nitrogen and carbon levels. Devastating changes in soil pH and C:N ratios can alter the composition of the microbiome
[25][97].
3. Plant Microbiome
To understand the defense mechanism in plants, one needs to study the plant–pathogen interaction. Many microbial communities and microbes have beneficial effects on their host plant. These microbes benefit the plants by improving nutrient acquisition and growth; providing resistance against pathogens; and y enhancing resistance against abiotic stresses, such as heat, drought, soil salinity, and many others. Somehow, beneficial microbes are often specific to a species cultivar. It was observed that few plant signals that trigger plant immune response can distinguish between pathogenic and beneficial microbes. However, it is still unclear which factors help a plant distinguish between beneficial and pathogenic microbes
[26][98]. Naturally, a plant’s habitat is a conducive environment for several microbes, including bacteria, oomycetes, fungi, archaea, and even pathogenic microbes. Plant microbiota composition is shaped by the complex multilateral interaction among microbes. Microbes exhibit commensal, pathogenic, and mutualistic relations with their host plants. The microbiome profiling of plants and looking at root-associated soils revealed the dynamic and diverse range of microbiomes. Many environmental factors (soil type, daylight, and season) and host factors (species and developmental stage) may affect the shape of bacterial communities. Soil and air act as physical barriers for plant-associated microbiomes
[27][99]. The phyllosphere is the aerial part of the plant and is a suitable habitat for microbes. The phyllospheric microbiome greatly affects the performance of the plant. These microbes also help to remove contaminants from plants. They also help to maintain plant health and suppress the growth of plant pathogens. The microbiota of plant parts that are far from the soil or in other aerial parts of plants are highly affected by the long-distance transport process. Highly beneficial and functionally significant microbes are found belowground. At the early stages of growth, microbial communities above the ground are highly influenced by the soil. Microbial communities are found abundantly in soil, with lower amounts in the rhizosphere portion and a more decreased proportion in the endophytic compartment. Four bacterial phyla were found to dominate around the rhizosphere and endosphere of plants: Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria
[28][100]. Members of bacterial communities have a strong influence on each other, as they can have antagonistic, mutualistic, and competitive interactions. Mostly, microbes interact by engaging in nutritional competition, exchange, and interdependence relations. The endosphere compartment of the plant has lower microbial diversity than rhizosphere. The microbial community of the root endosphere is more abundant than in the leaves. However, it is also known that entophytic microbes also play a significant role in plant development
[29][101]. The effect of the root bacterial microbiome on maize, barley, and
Arabidopsis thaliana in soil has been studied
[30][102]. Peiffer et al.
[31][103] observed that approximately 5–7% of the microbiome genotypes differ from the host genotype. These differences were mostly related to the quantitative nature, at a large scale, when maize rhizosphere microbiomes were studied. The microbiome was sampled during the growing season and then replicated after 5 years, showing that the root-associated microbiota was not changed. Only 143 operational taxonomic units (OTUs) were identified that correlated to the plant genotype
[32][104]. About 200 naturally occurring
Arabidopsis thaliana accessions have been screened in a single member of the rhizosphere community. Those accessions that were selected have been planted in natural soils; two of them could inhibit the growth of
Pseudomonadaceae. Thus, it can be concluded that even a single cultivar is enough to affect the structure of microbial communities. The rhizosphere is a significant zone between the plant’s root and soil microbiomes. The rhizosphere provides a suitable environment for both plant and microbial growth. The assemblage of microbiomes in the rhizosphere mostly depends on plant-derived metabolites
[33][105].
4. Microbe-Mediated Mitigation of Abiotic Stresses
For the survival of a plant in an environment with abiotic stress, one of the key adaptations is microbial interaction with the plant. Microbe-mediated induction of abiotic stress response is termed Induced Systemic Tolerance (IST). The microbiome helps plants mitigate abiotic stress by using their metabolic and genetic capabilities
[34][106]. It was observed that the most significant rhizospheric occupants that aid in the mitigation of various abiotic stresses in plants belong to the genera
Pseudomonas [35][107],
Azotobacter [36][108],
Azospirillium [37][109],
Rhizobium,
Pantoea,
Bacillus,
Enterobacter [35][107],
Bradyrhizobium [38][110],
Methylobacterium [39][111],
Burkholderia [40][112], and
Trichoderma [40][112] and the group cyanobacteria
[41][113]. To overcome crop productivity limitations, one of the viable methods is the selection, screening, and application of stress-tolerant microorganisms.
Trichoderma species have been thoroughly investigated in this regard. In one of the studies,
Trichoderma harzianum was used for the alleviation of stress in rice by upregulating aquaporin, dehydrin, and malonialdehyde
[42][114].
T. harzianum was also employed for the enhanced production of oil from NaCl-affected Indian mustard (
Brassica juncea). This, as shown in the results, also improved the nutrient uptake, enhanced the accumulation of antioxidants, and lowered the Na
+ uptake
[43][115]. Brotman et al.
[44][116] demonstrated that mutant
Trichoderma can mitigate salinity stress by the production of ACC-deaminase. In barley and oats, the production of IAA and ACC-deaminase seemed to be enhanced by the use of
Pseudomonas sp. and
Acinetobacter sp.
[45][117]. Simmons et al.
[46][118] used
Streptomyces sp. for the alleviation of salt stress and growth enhancement in the Micro-Tom tomato plant. Meanwhile, in maize and wheat, drought stress was ameliorated by using the strain
Burkholderia phytofirmans PsJN
[47][119]. Alteration in the levels of phytohormones, defense-related protein, enzymes, antioxidants, and epoxypolysaccharides is identified as Rhizobacteria-induced drought endurance and resilience (RIDER). These alterations make plants more resistant toward abiotic stresses
[48][120].
The soil microenvironment of the root region contains many microbes, as it harbors a diversity of nutrients, minerals, and metabolites. Substances secreted by a plant root significantly affect microbial colonization within the rhizosphere. Microorganisms move toward the root exudates by chemotactic movement. This movement acts as a dragging force for the colonization of microbial communities around the roots. PGPRs function as biofertilizers, phytostimulators, and biocontrol agents while harnessing the benefits of the rhizosphere/microenvironment. PGPRs depend upon their capabilities, interaction mode, and surrounding conditions. Plant growth is stimulated by bacteria through direct, as well as indirect, actions
[49][121]. Synthesis of bacterial compounds through the direct method is beneficial for the uptake of essential nutrients and micronutrients from the soil. These bacteria also help produce plant-growth regulators such as IAA, deaminase, and ACC, which help improve plant growth. These growth-promoting compounds enhance the growth and prevent stress ethylene from becoming overly inhibitory to plant growth
[50][51][122,123]. Moreover, the microbes help sequestrate iron and zinc, phosphorous and potassium solubilize, atmospheric nitrogen fixation, and plant hormone synthesis. However, on the other hand, the indirect mechanism shows antagonistic activity toward plant pathogenic organisms and the production of antifungal compounds
[52][64]. Bacterial metabolites act as extracellular signals to induce systemic resistance. This initiates a series of internal processes. The activation of plant defense mechanisms is triggered by the translocated signal received by distant plant cells. Another significant microbiome that acts as a plant-growth promoter is fungi, particularly mycorrhiza, either mycorrhizal fungi or vesicular-arbuscular mycorrhizal (VAM) fungi. These fungi form endosymbiotic associations with plants. Their hyphae form complex networking; thus, nutrient uptake by roots increases.
Salt tolerance in barley and drought tolerance in Chinese cabbage were found to be induced by the root fungal endophyte identified as
Piriformospora indica [53][124]. Microbes help plants maintain their growth and development, even under abiotic stress, and they also aid in the production of nutrients, hormones, and organic phytostimulant compounds. These actions of microbiomes make them strong and viable to fight against abiotic stress for plants. Various studies were carried out that elaborate on the role of microbiomes in the mitigation of abiotic stress for crop plants. Some soil-inhabiting microbes, such as
Achromobacter,
Azospirillum,
Variovorax,
Bacillus,
Enterobacter,
Azotobacter,
Aeromonas,
Klebsiella, and
Pseudomonas, help to enhance plant growth even under undesirable environmental conditions
[48][120]. Such soil bacteria that help plants to grow under abiotic stress have been classified as plant-growth promoters (PGP). Indole acetic acid (IAA) synthesized in plant shoots acts as plant-growth-regulating molecules. Auxins and IAA perform as a growth-stimulating effect, resulting in root-growth initiation, while a higher concentration of auxin negatively affects plant root growth
[35][107].
Table 1 presents a list of microbes and tolerance strategies used to control abiotic stress in plants. It was observed from recent studies that PGPRs not only help in the alleviation of abiotic stresses but also increase the plant crop yield of several crops, including rice, maize, barley, and soybean
[54][125].
Table 1.
Various tolerance strategies used to control abiotic stress in plants.
4.1. Mechanisms of PGPRs
The changes in the rhizosphere microbial community may cause plant-growth promotion by PGPRs
[70][140]. PGPRs use both direct and indirect modes of action for plant growth. Some PGPRs are strains of
Bacillus,
Rhizobium,
Acinetobacter,
Alcaligenes,
Azotobacter,
Arthrobacter,
Enterobacter,
Pseudomonas,
Serratia, and Burkholderia. In the direct mode of action, PGPRs include atmospheric nitrogen fixation, the production of phytohormones and enzymes in plants. Meanwhile, siderophores’ production, antibiotics’ production, and enzymes’ release (e.g., chitinase) are among the mechanisms of the indirect mode of action
[71][141].
4.2. Direct Mechanisms
In direct mechanisms, PGPRs help to promote plant growth in the absence of the pathogen. Rhizospheric microbial activity also affects the rooting and nutrient-availability pattern. Some direct mechanisms of PGPRs for plant growth are discussed hereunder.
Nitrogen fixation—The plant growth and productivity depend on the availability of vital nutrients such as nitrogen (N
2). Nitrogen-fixing microorganisms play an important role in biological nitrogen fixation under mild temperatures
[72][142]. Nitrogen-fixing organisms are classified into symbiotic and non-symbiotic N
2-fixing bacteria. Symbiotic N
2-fixing bacteria include leguminous and non-leguminous plants such as
rhizobia and
Frankia. Meanwhile, non-N
2-fixing bacteria refer to cyanobacteria such as
Nostoc,
Azotobacter, and
Azocarus [73][143]. The symbiosis connection may lead to the production of nodules
[74][144]. The nitrogen-fixation mechanism is carried out by an enzyme nitrogenase complex. For nitrogen fixation and the regulation of the enzyme, genetic control is present in such bacteria and nitrogenase genes are required. Meanwhile, for the synthesis and regulation of enzymes, regulatory genes are required; nitrogenase genes are also required. Moreover, regulatory genes are required to synthesize and regulate the enzymes. Structural genes are involved in activating Fe protein, iron–molybdenum cofactor biosynthesis, and electron donation
[75][145].
Phosphate Solubilization—Under stress conditions, plants usually face a shortage of nutrients such as phosphorous. It is mostly present in the soil in both forms, i.e., organic and inorganic
[76][146]. The shortage of phosphorous in plants occurs due to the presence of insoluble P in plants, but plants can only absorb it as monobasic and diabasic ions
[73][143]. Phosphate-solubilizing bacteria can work as a source of phosphorous in the form of biofertilizers. Some phosphate-solubilizing bacteria are
Azotobacter,
Microbacterium,
Bacillus,
Burkholderia,
Enterobacter,
Flavbacterium,
Erwinia,
Rhizobium, and
Serratia [77][147]. As plants cannot absorb inorganic P, Rhizobacteria have the potential to solubilize it, thus enhancing plant growth and yield. However, another cause of P solubilization could be due to the synthesis of organic acids by rhizospheric microorganisms
[78][148]. In plants such as the potato, tomato, wheat, and radish, phosphorous was solubilized by microbial species such as
Azotobacter chroococcum,
Enterobacter agglomerans,
P. putida,
Bradyrhizobium japonicum,
Cladosporium herbarum, and
Rhizobium leguminosarum [79][149].
Siderophore production—Iron is present abundantly in nature, but it is still unavailable for plants. Mostly, iron is found in the form of Fe
3+. PGPRs help to solubilize it by the secretion of siderophores, which are low-molecular-weight iron-binding proteins that help in the chelation of ferric iron (Fe
3+). The bacterial cell membrane dissolves siderophores and Fe
3+ in a 1:1 complex. This Fe
3+ is reduced to Fe
2+ and then released from siderophores to the cell. PGPRs enhance plant growth by releasing siderophores, which also help mitigate various plant diseases. Microbial siderophores act as a metal-chelating agent, which helps to control the iron availability in the rhizosphere
[80][150].
Phytohormone production—It is well-known that microbes help in the synthesis of phytohormone auxin, also known as indole-3-acetic acid (IAA). Many microorganisms that are isolated from multiple crops have the ability to synthesize IAA as a secondary metabolite
[81][151]. IAA plays a significant role in the interaction of rhizobacteria and plants
[82][152]. The synthesis of IAA affects plat cell division and helps to stimulate seed and tuber germination and the formation of adventitious roots. The secretion of bacterial IAA provides higher access for plants to nutrients by increasing their root surface area and length
[83][153]. Mostly,
Rhizobium species produce IAA, which upregulates cell division and the formation of vascular bundles. Several environmental stress factors, such as an acidic pH, osmotic stress, and carbon limitation, cause the modification of IAA synthesis in bacteria
[84][154].